Hantavirus
Hemorrhagic Fever with Renal
Syndrome (HFRS), Hantavirus
Pulmonary Syndrome (HPS),
Hemorrhagic Nephrosonephritis,
Epidemic Hemorrhagic Fever,
Korean Hemorrhagic Fever,
Nephropathia Epidemica (NE)
Last Updated: March 2009
Importance
Hantaviruses are a large group of viruses, carried in rodents and insectivores
worldwide, which can cause disease in people who become accidental hosts. Each virus
appears to have co-evolved with its reservoir host, and does not usually cause illness in
this animal. In humans, the consequences of infection depend with the virus. Although
some hantaviruses tend to be associated with asymptomatic infections or mild disease,
others have case fatality rates of 50% or greater. Hantavirus infections are fairly
common in parts of Asia and Europe. Although hantavirus-associated disease was first
reported in the United States in the 1990s during an outbreak in the Four Corners
region, these viruses are not new to the U.S. Since the 1990s, they have been reported in
rodents and insectivores throughout the country, and additional human cases have been
found. There is serologic evidence that some domesticated animals may also become
accidental hosts for hantaviruses, but little or no evidence of disease.
Etiology
Hantaviruses (genus Hantavirus, family Bunyaviridae) are a group of antigenically
distinct viruses carried in rodents and insectivores (shrews and moles). Each hantavirus
is endemic in one, or at most, a few specific rodent or insectivore hosts, to which it is
well adapted. At least 20 hantaviruses have been identified, but estimates of the exact
number of viruses vary. Newly identified hantaviruses are often named for the location
where the virus is found; however, some of these viruses are later reclassified. The
Laguna Negra, Rio Mamore, Oran, Lechiquanas and Pergamino viruses, which were
once thought to be separate hantaviruses, are now considered to be variants of Andes
virus, and the New York virus and Monongahela virus are currently classified as
variants of Sin Nombre virus. One variant of Dobrava virus (DOBV-Aa) is also called
Saaremaa virus; whether this is a separate virus or a less pathogenic variant of Dobrava
virus is controversial. Some hantaviruses have not yet been named.
Different hantaviruses cause hemorrhagic fever with renal syndrome (HFRS) and
hantavirus pulmonary syndrome (HPS), the two syndromes seen in humans.
Hemorrhagic fever with renal syndrome is a group of clinically similar diseases that
occur mainly in Europe and Asia. The most important hantaviruses causing HFRS are
Hantaan virus, Puumala virus, Dobrava virus and Seoul virus. Other hantaviruses
such as Amur virus are also associated with this disease. HFRS includes several
diseases that formerly had other names, including Korean hemorrhagic fever and
epidemic hemorrhagic fever. ”Nephropathia epidemica” is sometimes used for a mild
form of HFRS, which is often caused by Puumala virus or Saaremaa virus.
Hantavirus pulmonary syndrome is caused by a number of hantaviruses in North
and South America. In the United States and Canada, the Sin Nombre virus (with its
Monongahela and New York variants) is responsible for most cases. HPS can also
result from infection by the Muleshoe, Black Creek Canal and Bayou viruses , as well
as other named or unnamed hantaviruses. In South and Central America, Andes virus
and its variants are important causes of HPS, and Choclo, Castelo Dos Sonhos,
Juquitiba, Bermejo, Maciel and other hantaviruses can also cause this syndrome.
Some hantaviruses have yet been not been linked to human disease, either because
they are not pathogenic for humans or because their rodent hosts are unlikely to pass
the virus to humans.
Geographic Distribution
Hantaviruses are found worldwide in rodents and insectivores. The distribution of
each virus is usually limited by the geographic range of its specific host(s).
The viruses that cause hantavirus pulmonary syndrome seem to occur only in
North, Central and South America. Confirmed human cases have been reported in the
United States, Canada, and some countries in Central and South America. In the U.S.,
most cases are seen in the western states, but infections have been reported throughout
the country. Hantaviruses reported to cause HPS in North America include Sin Nombre,
Black Creek Canal, Muleshoe and Bayou viruses. Hantaviruses that have been
associated with HPS in South and Central America include Andes, Bermejo, Choclo,
Araraquara, Juquitiba, Maciel and Castelo dos Sonhos viruses.
© 2009
page 1 of 7
Hantavirus
HFRS is mainly seen in Europe and Asia; however,
one agent, the Seoul virus, can be found worldwide in its rat
host, and has been associated with a few cases of HFRS in
the United States. In addition to Seoul virus, HFRS is
caused by Hantaan virus in Asia, and by Dobrava and
Puumala viruses in Europe. Other viruses are also
associated occasionally with cases of HFRS.
Although clinical cases have not been reported from
Africa or the Middle East, antibodies to hantaviruses have
been reported among humans in both regions, and a
hantavirus was recently discovered in the African wood
mouse (Hylomyscus simus).There is currently no evidence
for hantavirus-associated disease in Australia, but it is
likely that hantaviruses are carried in some Australian
rodents or insectivores.
Transmission
Each hantavirus has one or possibly a few specific
rodent or insectivore hosts. In these host populations,
infections can be spread in aerosols and via bites. Other
routes of exposure may also be possible. Rodents can shed
hantaviruses in saliva, feces and urine. Infected animals
carry these viruses for weeks to years, and sometimes for
life. Transient infections are also possible. Recently
infected animals tend to shed larger amounts of virus;
generally, virus shedding decreases significantly by
approximately 8 weeks after infection. Transmission routes
may vary with the specific virus; for example, some
hantaviruses are more readily isolated from the urine than
others. Rodents do not appear to transmit Hantaan or
Puumala viruses vertically.
Humans can become incidental hosts when they
contact infected rodents or their excretions. Often, rodent
urine, droppings or nests are disturbed in enclosed areas;
the viruses are then inhaled in aerosolized dust. Infection
can sometimes occur after only a few minutes of exposure
to aerosolized virus. Hantaviruses can also be transmitted
through broken skin, the conjunctiva and other mucous
membranes, by rodent bites and possibly by ingestion.
Vertical transmission is generally thought to be negligible
or nonexistent; however, data suggesting the possibility of
hantavirus transmission in breast milk have been reported
from South America. Person-to-person spread has not been
seen in HPS cases in North America or HFRS in Eurasia,
but occurs occasionally with the Andes virus in Argentina.
In the environment, hantaviruses are susceptible to
drying, but can remain viable for longer periods if they are
protected by organic material. At room temperature (23°C;
73°F), both Puumala and Tula viruses lose viability within
24 h when they are dried, but can remain infectious for
more than 5 days if their environment remains moist. In cell
culture medium, these two viruses lose their infectivity
within 5–11 days at 23°C, but can survive up to 18 days at 4
°C (39°F). Both viruses are completely inactivated within
24 hours when they are kept at 37°C (98.6°F). Puumala
virus can remain infectious in the bedding of voles for 12Last Updated: March 2009
© 2009
15 days at room temperature. Hantaan virus also appears to
remain viable for several days at room temperature.
Whether animals other than rodents, shrews and moles
can shed hantaviruses is uncertain. Studies from China
suggest that hantavirus-infected pigs can excrete antigens in
urine and feces, and may also pass the virus to their
offspring across the placenta. Antibodies to hantaviruses
have been reported in other species, but they have not been
reported to shed these viruses. No infected animals have
been linked to human cases.
Most sources state that hantaviruses are not transmitted
by arthropods. However, experimental evidence for the
transmission of Hantaan virus by trombiculid mites
(chiggers, i.e., Leptotrombidium sp.), as well as evidence
for the occurrence of this virus in chiggers and gasmid
mites has been reported from China. RNA from Bayou
virus has been reported in mites and an ixodid tick in Texas.
The significance of these findings is unknown.
Disinfection
Hantaviruses are susceptible to many disinfectants
including 1% sodium hypochlorite, 2% glutaraldehyde,
70% ethanol and detergents. A 10% sodium hypochlorite
solution has been recommended for heavily soiled areas.
Hantaviruses are also susceptible to acid (pH 5) conditions.
In addition, they can be inactivated by heating to 60° C for
at least 30 minutes
Infections in Humans
Incubation Period
The incubation period for HFRS is 1-6 weeks.
Incubation periods of one week to 39 days and nine to 33
days have been reported in patients with HPS from Andes
virus and Sin Nombre virus, respectively.
Clinical Signs
Hantaviruses usually cause one of two diseases, HFRS
and HPS; however, other syndromes may also be possible.
Depending on the virus, hantavirus infections vary from
asymptomatic to severe.
Hemorrhagic fever with renal syndrome
The severity of HFRS varies with the causative agent.
Hantaan, Dobrava and Amur virus infections usually cause
severe symptoms. Seoul virus generally results in more
moderate disease, while Puumala and Saaremaa (Dobrava
Aa) virus infections are typically mild. Classically, the
course of the disease has been divided into febrile,
hypotensive/ proteinuric, oliguric, diuretic and convalescent
stages; these stages are usually more evident in severe
disease, and may not be seen in mild cases.
The onset of HFRS is usually abrupt; the initial clinical
signs may include fever, chills, prostration, headache and
backache. Gastrointestinal signs including nausea, vomiting
and abdominal pain may also be seen; in some cases, the
page 2 of 7
Hantavirus
pain can be severe enough to mimic appendicitis. Patients
may also develop injected mucous membranes, photophobia,
temporary visual impairment, a flushed face and
conjunctivae, or a petechial rash, which usually occurs on the
palate or trunk. This prodromal stage typically lasts for a few
days to a week, and is followed by the onset of renal signs.
The first stage is the proteinuric stage. Hypotension may
develop during this phase of the disease and can last for
hours or days. Nausea and vomiting often occur, and death
may result from acute shock. In severe cases, this is typically
followed by an oliguric phase then a diuretic/polyuric phase
as kidney function improves. Death can occur at any point,
but it is particularly common during the hypotensive or
oliguric phases. In severe cases, kidney failure may be seen.
Some cases have lung involvement (to a lesser extent than in
HPS) or neurological signs. Hemorrhagic signs or
tendencies including petechiae, hematuria or melena may
also be seen, particularly in more severe cases.
Disseminated intravascular coagulation can occur. Full
recovery may take weeks or months, but patients usually
recover normal kidney function. Rare complications may
include chronic renal failure and hypertension.
Hantavirus pulmonary syndrome
Hantavirus
pulmonary
syndrome
is
usually
characterized by pulmonary rather than kidney disease. The
initial phase usually lasts for 3 to 5 days; the clinical signs
during this period are similar to the prodromal stage of
HFRS, and may include fever, myalgia, headache, chills,
dizziness, malaise, lightheadedness, nausea, vomiting and
sometimes diarrhea. Arthralgia, back pain and abdominal
pain are occasionally seen. Respiratory distress and
hypotension usually appear abruptly, with cough and
tachypnea followed by pulmonary edema and evidence of
hypoxia. Cardiac abnormalities can occur, and may include
bradycardia, ventricular tachycardia or fibrillation. After the
onset of the cardiopulmonary phase, the disease usually
progresses rapidly; patients may be hospitalized and require
mechanical ventilation within 24 hours. Kidney disease can
also be seen, but it tends to be mild; kidney damage occurs
more often with the Andes, Bayou and Black Creek viruses.
Hemorrhagic signs are rare in patients with HPS in North
America, but more common in South America. Although
recovery is rapid and patients usually recover full lung
function, convalescence may last for weeks or months.
Asymptomatic or mild infections appear to be rare with Sin
Nombre virus, but may be more common with some South
American hantaviruses. Andes virus infections tend to
cause severe disease, while Choclo virus infections are
usually milder.
Other syndromes
Mild cases can have a variety of signs and symptoms
that do not necessarily resemble HPS or HFRS. Hantavirus
infections have been suspected in fever of unknown origin
in some Asian countries. In Europe, Tula virus infections
were found in two patients. One case occurred in a 12-yearLast Updated: March 2009
© 2009
old boy in Switzerland who had been bitten by a rodent and
developed paronychia, recurrent febrile episodes, a slightly
enlarged spleen and a macular, nonpruritic rash on his torso
and proximal limbs. The other patient was an adult with
fever, renal disease and pneumonia. The Tula virus
infection was suspected but not proven to be the cause of
the disease in both cases.
Communicability
Although viruses can be found in the blood and urine
of HFRS patients, person-to-person transmission has not
been seen in cases of HPS in North America or HFRS in
Eurasia. Person-to-person transmission has been reported
during at least two outbreaks of Andes virus in South
America. One study suggested that transmission might take
place during the prodromal stage of illness or shortly
afterward.
Diagnostic Tests
A definitive diagnosis can be made if the hantavirus is
isolated from the patient; however, recovery is not always
successful. In addition, some hantaviruses (including Sin
Nombre virus) have never been isolated in cell culture. If
viruses are found, they can be identified by virus
neutralization.
Hantavirus infections are often diagnosed by serology.
Either the presence of specific IgM in acute phase sera or a
rise in IgG titer is diagnostic. Serological tests include the
immunofluorescent antibody test (IFA), enzyme-linked
immunosorbent assays (ELISA), immunoblotting and virus
neutralization. Commercial ELISA and/or immunoblot
assay kits have been developed for Dobrava, Hantaan,
Puumala, Seoul, Sin Nombre and some other viruses. Rapid
immunochromatographic IgM antibody tests have been
described in the literature for acute Dobrava, Hantaan and
Puumala virus infections. Hantaviruses can cross-react in
some serologic assays.
Hantavirus infections can also be diagnosed by finding
antigens in tissues with immunohistochemistry. Viral RNA
can be detected in blood or tissues with reverse
transcriptase- polymerase chain reaction assays (RT-PCR).
PCR assays that can differentiate some hantaviruses have
been described; one published assay identifies Dobrava,
Hantaan, Seoul and Puumala viruses. Real-time RT-PCR
has been described for some viruses.
Treatment
Supportive care is the mainstay of treatment. Intensive
care may be required. Ribavirin may be helpful in cases of
HFRS, but has not been effective for HPS to date.
Prevention
Hantavirus infections can be prevented by avoiding
exposure to rodents and their excretions. Many cases of
HPS and HFRS occur after living or working in an
enclosed, rodent-infested space; however, some patients
page 3 of 7
Hantavirus
have reported no known contact with rodents or their feces.
HFRS has also been associated with agricultural activities,
such as harvesting crops or working with hay. Homes,
sheds and other buildings should be rodent-proofed, and
food should be stored securely to avoid attracting these
pests. When complete rodent-proofing is impossible, traps
or rodenticides should also be used for control.
The Centers for Disease Control and Prevention (CDC)
website has information on the safe cleaning of rodentinfested areas and droppings. Precautions include airing out
the room before starting clean-up, and wetting the area with
commercial disinfectant or bleach. Infested areas should be
cleaned with paper towels, followed by mopping or
sponging. Procedures that might aerosolize the virus, such
as sweeping, should be avoided, and protective clothing and
gloves should be worn while cleaning. Special precautions
must be taken when cleaning heavily infested areas; a local,
state or federal health department should be contacted for
detailed guidelines.
People who are occupationally exposed to rodents
should take additional precautions to prevent infection.
Depending on the circumstances and type of exposure, this
may include gloves, goggles, rubber boots or disposable
shoe covers, coveralls or gown, and/or a respirator (as of
2008, the CDC recommends a N-100 filter type respirator).
In the U.S., detailed precautions for a variety of situations,
including exposure to rodent blood and organs, are
available from the CDC. Anyone who develops a febrile
illness consistent with the early signs of HPS or HFRS
should seek medical attention promptly, and inform the
attending physician of the occupational risk. Hospitals
should follow universal precautions when treating patients
with Andes virus infections. People who have been in
contact with these patients should be monitored for
prodromal symptoms.
Vaccines for hantaviruses are in development, but are
not yet available in the U.S. One commercial inactivated
vaccine for HFRS (Hantavax) is available in Korea, but
some studies suggest the protection is incomplete.
Morbidity and Mortality
Hantavirus outbreaks are often associated with
increased rodent populations or environmental factors that
lead to increased human exposure to rodents. HPS tends to
peak in late spring or early summer. HFRS tends to peak
with human agricultural activities in spring and fall.
Occupations that may be at higher risk of infection include
rodent control workers, field biologists/ mammalogists,
farmers, forestry workers and military personnel. Activities
such as camping or staying in rodent-infested cabins can
also increase the risk.
Approximately 1-8% of the population has antibodies
to hantaviruses in Europe; the seropositivity rate varies with
the country and specific virus. Worldwide, approximately
150,000 to 200,000 people are hospitalized with HFRS each
year, mainly in Asia. In Europe, HFRS is most common in
Last Updated: March 2009
© 2009
Russia (3000 cases), Finland (1000 cases) and Sweden (300
cases), with 100 or fewer cases seen annually in other
countries. In the U.S., 0.2-0.5% of the general population is
seropositive for hantaviruses. One study reported that 0.5%
(4 of 757) of active mammalogists working in the field had
antibodies to Sin Nombre virus; one of the four seropositive
individuals reported being hospitalized for an illness
suggestive of HPS. As of March 2007, fewer than 500 cases
of HPS have been reported in the U.S. since the Sin
Nombre virus was discovered. In South America, 1-40% of
the population has antibodies to hantaviruses, and HPS is
also more common.
Different hantaviruses tend to cause mild, moderate or
severe disease. The mortality rate also varies with the
availability of healthcare services. The case fatality rate is
approximately 0.1% to 0.4% for Puumala virus (the most
commonly reported infection in Europe), 1-5% for Seoul
virus, 7-12% for Dobrava virus, and 10-15% for Hantaan
virus. The estimated case fatality rate is 40-60% for HPS
caused by Sin Nombre virus. The case fatality rate for
Muleshoe, Black Creek Canal and Bayou viruses is also
greater than 40%. Andes virus infections have a similar
case fatality rate (43-56%), but the mortality rates for some
variants may be lower: the case fatality rate is 9-29% for
Laguna Negra virus and 8-40% for Lechiguanas virus and
Oran virus. Choclo virus infections have a case fatality rate
of approximately 25%.
Infections in Animals
Hantaviruses in Rodents and Insectivores
Hantaviruses are found naturally in various species of
rodents and insectivores (shrews and moles). Each virus is
thought to be carried mainly by one species of animal;
however, sometimes a species can carry more than one
hantavirus, and some hantaviruses may infect more than
one host. The infection rate varies between sites and over
time, but in some cases, up to 50% of a rodent population
can be seropositive. On average, approximately 10% of
deer mice are seropositive for Sin Nombre virus.
Hantaviruses can be carried lifelong, and are not
usually associated with overt disease in their reservoir
hosts. However, studies have reported decreased survival in
bank voles (Myodes glareolus) infected with Puumala virus
and deer mice infected with Sin Nombre virus, as well as
lower weight gains in infected male deer mice.
Domesticated rodents can develop clinical signs when they
are infected with some hantaviruses. Hamsters infected with
Andes virus may develop fatal pulmonary disease similar to
HPS. Hantavirus infections can also kill neonatal rodents.
Fatal meningoencephalitis occurs in infant laboratory mice
(Mus musculus) experimentally infected with Hantaan
virus, as well as rats infected with Seoul virus. Maternal
antibodies seem to be protective during the period of
susceptibility. Rats and mice over the age of 2-3-weeks do
not usually develop clinical signs. Infant mice do not seem
page 4 of 7
Hantavirus
to be susceptible to disease caused by Puumala or Sin
Nombre viruses.
To prevent infections in laboratory colonies, wild
rodents should be quarantined and tested for hantaviruses.
This may be particularly important in some regions. One
study from Korea reported serologic evidence for
hantaviruses in 12% of rats and 23% of mice in
conventional facilities, and 3% of mice in barrier facilities.
Serology, immunoblotting of lung or other tissues for
antigens, and RT-PCR can be used to detect hantavirus
infections in rodents.
Hantaviruses in Other Mammalian
Species
Species other than rodents and insectivores can be
infected by hantaviruses, but there is little or no evidence
that these animals become ill. Antibodies to some
hantaviruses have been found in cats, dogs, swine, horses,
cattle, deer, rabbits/ hares, chipmunks and moose. In one
study, 10% of healthy cats in the United Kingdom and 23%
of cats with chronic diseases were seropositive. Other
studies have reported lower rates. Horses, cattle and coyotes
were seronegative in one U.S. survey.
Pigs were reported to be systemically infected with
hantaviruses in China. Hantavirus antigens were found in
the heart, liver, lung, spleen, kidney, blood, urine and feces,
as well as in wastes from pigpens. A Russian study reported
that hantavirus antigens could be found in the lungs of
several avian species (including passerine birds, pheasants,
doves, herons and owls) in the far eastern region of the
country; this finding remains to be confirmed.
Cynomolgus macaques (Macaca fascicularis) that were
experimentally infected with Puumala virus became lethargic
and developed kidney disease with proteinuria and
microhematuria. When cynomolgus macaques were infected
with Andes virus, they did not have clinical signs but did
have transient decreases in lymphocyte numbers. Disease has
not been associated with hantaviruses in other species.
Internet Resources
Centers for Disease Control and Prevention (CDC). Rodent
Control.
http://www.cdc.gov/rodents/
CDC. All About Hantavirus. Technical Information Index.
http://www.cdc.gov/ncidod/diseases/hanta/hps/noframe
s/phys/technicalinfoindex.htm
Public Health Agency of Canada. Material Safety Data
Sheets
http://www.phac-aspc.gc.ca/msds-ftss/index.html
Medical Microbiology
http://www.ncbi.nlm.nih.gov/books/NBK7627/
The Merck Manual
http://www.merck.com/pubs/mmanual/
Last Updated: March 2009
© 2009
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Hantavirus
Table 1: Selected hantaviruses and their major rodent hosts
Virus
Rodent Host(s)
Virus
Rodent Host(s)
Amur
Apodemus peninsulae
Juquitiba
Oligoryzomys nigripes
Andes
Oligoryzomys longicaudatus
(long-tailed pygmy rice rat)
Calomys laucha
Khabarovsk
Microtus fortis
(reed vole)
Sigmodon hispidus (cotton rat)
Laguna Negra
(Andes virus variant)
Lechiguanas
(Andes virus variant)
Oran
(Andes virus variant)
Rio Mamore
(Andes virus variant)
Araraquara virus
Asama virus
Ash River
Bayou
Black Creek Canal
Bloodland Lake
Camp Ripley
Choclo
Dobrava
El Moro Canyon
Hantaan
Hu39694
Muleshoe
Prospect Hill
Oligoryzomys flavescens
Puumala
Oligoryzomys longicaudatus
Rio Segundo
Oligoryzomys microtis
(small-eared pygmy rice rat)
Bolomys lasiurus
Saaremaa (or
DOBV-Aa)
Seewis
Urotrichus talpoides
(Japanese shrew mole)
Sorex cinereus
(masked shrew)
Oryzomys palustris
(rice rat)
Sigmodon hispidus
(cotton rat)
Microtus ochrogaster
(prairie vole)
Blarina brevicauda
(northern short-tailed shrew)
Oligoryzomys fulvescens
(fulvous pygmy rice rat)
Apodemus flavicollis
(yellow-necked field mouse)
Reithrodontomys megalotis
(Western harvest mouse)
Apodemus agrarius
(striped field mouse)
Oligoryzomys flavescens (?)
Seoul
Sin Nombre
Monongahela
(Sin Nombre virus
variant)
New York
(Sin Nombre virus
variant)
Soochong
Microtus pennsylvanicus
(meadow vole)
Myodes glareolus
(bank vole)
Reithrodontomys mexicanus
(Mexican harvest mouse)
Apodemus agrarius
(striped field mouse)
Sorex araneus
(Eurasian common shrew)
Rattus norvegicus
(Norway rat);
Rattus rattus
(black rat)
Peromyscus maniculatus
(deer mouse)
Peromyscus maniculatus
(deer mouse)
Peromyscus maniculatus
(deer mouse);
P. leucopus
(white-footed mouse)
Apodemus peninsulae
Tanganya
Crocidura theresae
(Therese shrew)
Thailand
Bandicota indica
(bandicoot rat)
Thottapalayam
Suncus murinus
(musk shrew)
Isla Vista
Microtus californicus
(California vole)
Topografov
Lemmus sibiricus
(Siberian lemming)
Jemez Springs
Sorex monticolus
(dusky shrew )
Tula
Microtus arvalis
(European common vole)
Last Updated: March 2009
© 2009
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